Distinct context-and content-dependent population codes in superior colliculus during sensation and action

Abstract

Sensorimotor transformation is the process of first sensing an object in the environment and then producing a movement in response to that stimulus. For visually guided saccades, neurons in the superior colliculus (SC) emit a burst of spikes to register the appearance of stimulus, and many of the same neurons discharge another burst to initiate the eye movement. We investigated whether the neural signatures of sensation and action in SC depend on context. Spiking activity along the dorsoventral axis was recorded with a laminar probe as Rhesus monkeys generated saccades to the same stimulus location in tasks that require either executive control to delay saccade onset until permission is granted or the production of an immediate response to a target whose onset is predictable. Using dimensionality reduction and discriminability methods, we show that the subspaces occupied during the visual and motor epochs were both distinct within each task and differentiable across tasks. Single-unit analyses, in contrast, show that the movement-related activity of SC neurons was not different between tasks. These results demonstrate that statistical features in neural activity of simultaneously recorded ensembles provide more insight than single neurons. They also indicate that cognitive processes associated with task requirements are multiplexed in SC population activity during both sensation and action and that downstream structures could use this activity to extract context. Additionally, the entire manifolds associated with sensory and motor responses, respectively, may be larger than the subspaces explored within a certain set of experiments.